Receptor-based protein binding in the supramolecular network of velvet worm slime

The slime of velvet worms (Onychophora) is a protein-based bioadhesive that undergoes rapid, yet reversible transition from a fluid into stiff fibers used for prey capture and defense, but the mechanism by which this phase transition functions is largely unknown. Here, integrating transcriptomic and proteomic approaches with AI-guided structure predictions, we discover a group of evolutionarily conserved leucine-rich repeat (LRR) proteins in velvet worm slime that readily adopt a receptor-like, protein-binding "horseshoe" structure. Our structural predictions suggest dimerization of LRR proteins and support their interactions with conserved {beta}-sheets-rich domains of high-molecular-weight proteins, the primary building blocks of velvet worm slime fibers. This previously unknown functional context of LRR proteins is presumably involved in reversible, receptor-based supramolecular network formation in these adhesive biofibers and provides possible new avenues for fabricating fully recyclable (bio)polymeric materials. Significance StatementAnalyzing structure-function-relationships underlying reversible fiber formation in velvet worm slime may inspire avenues for the sustainable fabrication of protein-based polymeric materials. Here, we present evidence for an evolutionarily conserved mechanism of reversible fiber formation in velvet worm slime based on the receptor-like binding of fiber forming proteins by a leucine-rich repeat (LRR) protein. The structures of both protein components are highly conserved evolutionarily in the two distantly related velvet worm subgroups, indicating pervasive presence of this mechanism across species that has been maintained through the last [~]380 MY. Our results suggest that the ubiquitously occurring LRR motif--better known for its innate immunity and developmental roles--has a novel identified function in processing a biological material, which might contribute to the development of sustainable bio-inspired materials.